A Comparison of Flight Energetics and Kinematics of Migratory Brambling

Home , Brambling, Eurasian tree sparrow, Montifringilla

Wang et al. Avian Res (2020) 11:25 https://doi.org/10.1186/s40657-020-00211-y Avian Research

RESEARCH Open Access A comparison of fight energetics and kinematics of migratory Brambling and residential Eurasian Tree Sparrow Yang Wang1 , Yuan Yin1 , Zhipeng Ren1 , Chuan Jiang1 , Yanfeng Sun2 , Juyong Li1 , Ghulam Nabi1 , Yuefeng Wu1 and Dongming Li1*

Abstract Background: Unlike resident birds, migratory birds are generally believed to have evolved to enhance fight efciency; however, direct evidence is still scarce due to the difculty of measuring the fight speed and mechanical power. Methods: We studied the diferences in morphology, fight kinematics, and energy cost between two passerines with comparable size, a migrant (Fringilla montifringilla, Brambling, BRAM), and a resident (Passer montanus, Eurasian Tree Sparrow, TRSP). Results: The BRAM had longer wings, higher aspect ratio, lower wingbeat frequency, and stroke amplitude compared to the TRSP despite the two species had a comparable body mass. The BRAM had a signifcantly lower maximum speed, lower power at any specifc speed, and thus lower fight energy cost in relative to the TRSP although the two species had a comparable maximum vertical speed and acceleration. Conclusions: Our results suggest that adaptation for migration may have led to reduced power output and maximum speed to increase energy efciency for migratory fight while residents increase fight speed and speed range adapting to diverse habitats. Keywords: Flight energy efciency, Flight kinematics, Flight speed, Maximum load-lifting capacity

Background example, migratory birds not only have highly efcient Flight performance is a fundamental factor for ftness in wings (more prolonged and narrower wings, lower wing ecological and evolutionary contexts (Webster et al. 2002; loading) but also exhibit lowered wingbeat frequency Bauer and Hoye 2014). According to the theory of migra- and stroke amplitude for continuous fight avoiding addi- tion syndrome (Bauchinger et al. 2005; Hedenström tional parasite drag relative to residents (Minias et al. 2008), migratory birds have evolved a suite of modifca- 2015; Grilli et al. 2017). Given that it is difcult to directly tions in wing morphology and kinematics in terms of measure these parameters under the natural conditions energy consumption for long-journey fight than resi- (Zhao et al. 2017; Horton et al. 2018), little information dents (Hedenström 2008; van Oorschot et al. 2016). For is available on how migratory birds adjust airspeed and mechanical power relative to residents.

*Correspondence: [email protected] Considering that power consumption follows a 1 Key Laboratory of Animal Physiology, Biochemistry and Molecular U-shaped relationship with fight speed, fy at a speed too Biology of Hebei Province, College of Life Sciences, Hebei Normal low or high than usual will demand an extra amount of University, Shijiazhuang 050024, China Full list of author information is available at the end of the article energy and lower energy efciency (Alerstam et al. 2007;

© The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativeco mmons.org/licen ses/by/4.0/ . The Creative Commons Public Domain Dedication waiver (http://creativeco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Wang et al. Avian Res (2020) 11:25 Page 2 of 9

Alerstam 2011). Teoretically, small migratory birds × Pfght/Vmr, i.e., power cost per 100 km per unit body should fy at speed with the maximum range speed (Vmr) mass) can provide a framework to investigate the air- and maximize the efciency of fight to meet the strategy borne energy consumption of transport. Measuring the of energy-minimization during the fight (Hedenström vertical speed, acceleration during load-free fight tri- 2002; Tobalske et al. 2003). By contrast, residents are less als, and power margin (the excess available aerodynamic constrained by the energy demand of long-distance fight, power for vertical ascent) can evaluate the maneuverabil- and a higher maximum speed (Vmax) can improve chasing ity of birds (Altshuler et al. 2004). and escaping ability (Clemente and Wilson 2016, Fig. 1). Passerines (Passeriformes, Aves) are typically featured Te maximum load-lifting capacity experiment (as with fapping fight that have higher power requirements imposed via asymptotic loading) is a quantifable way to than those birds with other fight modes (e.g., soaring, determine maximum fight performance and estimate gliding). Terefore, passerines are under more selective maximum power available during the fight in volant pressures of optimizing fight speed and energy con- animals (Marden 1987; Altshuler et al. 2010). By meas- sumption (Gavrilov 2011; Vincze et al. 2018). To test uring fight-related morphology, kinematics, and maxi- the hypothesis that migrants would enhance the energy mum weight lifted during maximum load-lifting fight efciency at Vmr, and residents would have high Vmax to trials, we can calculate aerodynamic power output with improve maneuverability (Chernetsov 2012). We com- aerodynamic model and estimate fight speed (Vmr and pared the diferences in fight speed and energy efciency Vmax). Specifcally, Vmr is calculated with fight-related between two passerines with a resident species (Passer morphology and optimized kinematics; Vmax is the maxi- montanus, Eurasian Tree Sparrow, TRSP) and a migra- mal fight speed supported by maximal available output tory species (Fringilla montifringilla, Brambling, BRAM). power in load-lifting fight trials (Pennycuick 2008). Te We predicted that (1) BRAM would have a higher minimal fight energy cost at a certain distance (Distance Vmr and a better fight efciency to meet the time- and

Fig. 1 The relationship between airspeed and the aerodynamic power requirement during fight (Pennycuick 2008; Klein et al. 2015). At minimum

speed (Vmin) and maximum speed (Vmax), the required aerodynamic power equals the maximum available power output. At minimum power speed (Vmp) is when the required aerodynamic power is minimal (the speed for maximum endurance). At maximum range speed (Vmr) is when the cost of transport is minimal (the speed for maximum range) Wang et al. Avian Res (2020) 11:25 Page 3 of 9

energy- minimization of migration (Alerstam 2011); laboratory for determining their maximum fight capac- (2) TRSP would fight at a higher Vmax to achieve bet- ity within 2‒4 h. ter maneuverability for local competition and anti-pre- dation, with a lower fight efciency (Askew and Ellerby Maximum load‑lifting assay and wing kinematics 2007). Each bird was evaluated for asymptotic load-lifting capacity in a rectangular fight chamber using a maxi- Methods mum load-lifting approach described in detail by Sun Study species et al. (2016) and Wang et al. (2019). In brief, one high- speed video camera (GCP100BAC, JVC Kenwood Cor- Te BRAM is a small passerine migrant which can poration, Yokohama, Japan; operated at 250 frames−1) migrate as far as 3600 km (Fang et al. 2008; see distribu- placed on the top of the chamber was used to obtain tion map in Fig. 2) with comparable body size (~ 21 g), wingbeat frequency and stroke amplitude (Additional similar diets (seeds and invertebrates), and habitats (for- fle 1: Movie S1). Te other synchronized camera (oper- ests, shrublands, and artifcial; Snow and Perrins 1998; ated at 50 frames −1) positioned laterally at a distance Summers-Smith 2016) as the TRSP (common resident of 80 cm to the chamber was used to record the beads species with broad distribution range, Sun et al. 2017; Li remaining on the chamber foor during the maximum et al. 2019). load-lifting fight (Additional fle 2: Movie S2). Te maximum lifted weight was calculated by the total Birds collection weight of beads subtraction to the weight of remain- Te TRSP (n = 13) and BRAM (n = 8) were captured ing beads on the chamber foor when peak lifting was opportunistically using mist nets from March 13 to achieved. Te sum of bodyweight gave the maximum April 1, 2017, at the campus of Hebei Normal University load (total lifted load) and the maximum lifted weight. (37°59.88ʹN, 114°31.18ʹE, elevation: 72 m), Shijiazhuang, A time-averaged wingbeat frequency was determined China. Within 30 min post-capture, body mass was by the interaction frequency between wing motions and measured with a portable digital balance for each bird the camera flming speed over the same measurement to the nearest 0.01 g and transferred to the university period. Wing stroke amplitude was derived from video

Fig. 2 Breeding and non-breeding distribution ranges of Fringilla montifringilla (Brambling, BRAM; extracted from BirdLife International 2019) Wang et al. Avian Res (2020) 11:25 Page 4 of 9

Table 1 Statistical results of fight-related morphology, load-lifting capacity, fight kinematics, fight speed and energy efciency between Fringilla montifringilla (Brambling, BRAM; n 8) and Passer montanus (Eurasian Tree Sparrow, TRSP; = n 13) in independent t-tests or Mann–Whitney U tests = Type of variable Variable t value P value

Flight-related morphology Body mass (g) 0.569 0.576 Wing length (mm) 16.69 < 0.001 Wing area (cm2) 6.158 < 0.001 Wing loading (N/m2) 4.326 < 0.001 Aspect ratio 5.024 < 0.001 Load-lifting capacity Maximum load (g) 1.321 0.202 Mass-corrected maximum load 2.040 0.056 Maximum wing loading (N/m2) 4.326 < 0.001 Flight kinematics Wingbeat frequency (Hz) 6.627 < 0.001 Wing stroke amplitude (deg) 2.691 0.015 Flight performance Maximum vertical speed (m/s) 0.625 0.540 Maximum vertical acceleration (m/s2) 0.171 0.866 Power margin 0.641 0.529

Maximum range speed (Vmr, m/s) 8.298 < 0.001

Maximum speed (Vmax, m/s) 8.176 < 0.001 a Flight energy efciency Power at Vmr (W) 5.914 < 0.001

Power at Vmax (W) 6.266 < 0.001

Mass-corrected power at Vmr (W/kg) 6.669 < 0.001

Mass-corrected power at Vmax (W/kg) 7.228 < 0.001

Parasitic drag at Vmr (N) 5.972 < 0.001

Parasitic drag at Vmax (N) 5.817 < 0.001

Reynolds number at Vmr 3.336 0.003

Reynolds number at Vmax 3.411 0.003 a Mass-corrected power cost per 100 km at Vmr (Wh/kg) 7.901 < 0.001

Mass-corrected power cost per 100 km at Vmax (Wh/kg) 9.544 < 0.001 Italic values indicate signifcance of P value (P < 0.05) a Variables were compared by the Mann–Whitney U test

images in which the wings were located at the extreme dividing the body weight by S, and maximum wing load- positions of the wingbeat within each bout of fnal 0.5 s ing was provided by dividing the total maximum load of maximum load-lifting. Multiple ascending fights by S. Mass-corrected maximum load was calculated by were recorded for each bird (mean of 4.1 fights), and the dividing the total maximum load by body weight. maximum weight lifted within the series was assumed to indicate the limit to load-lifting of fight performance. All Flight speed and energy efciency birds were released after completing all measurements We measured the vertical speed for each individual based and fight trails (5‒6 h post-capture). on video records of load-free fight trials in the chamber. Te whole distance from the foor to the up limits of Flight‑related morphology the fight trials was evenly divided by four or fve parts Following load-lifting experiments, fight-related mor- with a length of 20 cm for each part. Te maximum ver- phological traits were measured to the nearest 0.1 mm tical speed and acceleration were calculated as the high- using Vernier caliper (Mitutoyo, Kawasaki, Japan). Te est achieved speed and acceleration among all parts for right-wing of each bird was photographed for measure- each individual. Maximum power (maximum available ments of the total wing area S (given by twice the area of muscle power to support the fight) during the maximum the right-wing) and wing length R using ImageJ (National load-lifting fight was calculated using Ellington’s equa- Institutes of Health, Bethesda, MD, USA). Te aspect tion (Ellington 1984) following the method described by 2 ratio is given by 4R /S. Wing loading was calculated by Askew and Ellerby (2007). Teoretical Vmr, Vmax, parasite Wang et al. Avian Res (2020) 11:25 Page 5 of 9

Fig. 3 Comparisons of a wing length (mm), b wing area (cm2), c aspect ratio and wing loading (kg/m2) and d wingbeat frequency (Hz) and wing stroke amplitude (degree) during the maximum load-lifting fight of Passer montanus (Eurasian Tree Sparrow, TRSP, n 13) and Fringilla montifringilla = (Brambling, BRAM, n 8). All variables difered signifcantly between species. All values depicted for each species are the means with standard error, = * represents P < 0.05. Images of each species were taken from https://www.hbw.com/

drag, Reynolds number, and the airborne energy ef- Results ciency of transport at Vmr and Vmax were calculated using Te BRAM and TRSP had a comparable body mass, max- computeFlightPerformance functions in “afpt” package imum load, and mass-corrected maximum load. How- for each individual (Klein et al. 2015) in R software (R ever, BRAM had signifcantly longer and larger wings, Core Team 2018). Te power margin was calculated as higher aspect ratio, smaller wing loading, lower wingbeat the diference of maximum power and minimum power frequency, and stroke amplitude compared with TRSP required to fight as an estimate of maneuverability. (Table 1; Fig. 3). Te BRAM and TRSP had a comparable maximum ver- Statistical analysis tical speed and acceleration, and power margin (Table 1). However, BRAM had a signifcantly lower V and V , Te homogeneity of variances was tested using Levene’s mr max power, parasitic drag, Reynolds number, and mass- test of equality of variances before analysis. We imple- corrected power cost per 100 km in both V and V mented independent t-tests or Mann–Whitney U tests mr max compared with those of TRSP (Table 1; Figs. 4 and 5). to compare all the variables between species. Statistical Furthermore, the BRAM had lower fight power, mass- analysis was performed using SPSS Statistics 21.0 soft- corrected fight power, and mass-corrected fight power ware (IBM, New York, USA). All data are presented as per 100 km relative to TRSP at low- and middle-speed mean SEM. Te signifcant diference was P < 0.05. ± ranges (Fig. 5). Wang et al. Avian Res (2020) 11:25 Page 6 of 9

Fig. 4 Comparisons of a fight speed (m/s), b fight power (W), c parasite drag (N), d Reynolds number, e mass-corrected power (W/kg), and f

mass-corrected power cost per 100 km (Wh/kg) at maximum range speed (Vmr) and maximum speed (Vmax) of Passer montanus (Eurasian Tree Sparrow, TRSP, n 13) and Fringilla montifringilla (Brambling, BRAM, n 8). All values depicted for each species are the means with standard error, * = = represents P < 0.05

Discussion in BRAM with lower power requirements (or available By identifying the diferences in fight-related morphol- power) when fying at any given speed relative to the ogy, load-lifting capacity, kinematics, and theoretical TRSP, especially at low- and middle-speed ranges (Fig. 5). fight speed and energy efciency between BRAM and More importantly, our results found that it is a dilemma TRSP, we found a signifcantly lowered Vmr and Vmax in for birds to enhance fight speed and efciency. Tere- BRAM relative to TRSP due to reduced power availabil- fore, the fight ability of small passerine migrants was ity (Fig. 4). Te trade-of between time and energy cost more constrained by energy rather than time (lower fight during migration is infuenced by body size (Zhao et al. speed and higher energy efciency). 2017), season (Nilsson et al. 2013), distance (Schmal- Te wing morphology and behavior of the wing motion johann 2018), etc. Our results suggested that migrant of birds are crucial components of powered fight perfor- passerines may be favored by a higher fight efciency mance and energy efciency (Alerstam 2011). Morpho- to achieve an energy- minimization strategy rather than logically, BRAM had larger and longer wings, and lower a time-minimization strategy, while residents may be wing loading relative to TRSP. Our results confrm that favored by a higher Vmax to achieve better maneuverabil- the avian wing has evolved to adapt to their various life- ity. Furthermore, the fight energy efciency was higher styles (Dudley 1991; Lockwood 1998). In comparison, Wang et al. Avian Res (2020) 11:25 Page 7 of 9

Fig. 5 Comparisons of a fight power (N), b mass-corrected power (W/kg), and c mass-corrected power cost per 100 km (Wh/kg) at a range of possible speed for Passer montanus (Eurasian Tree Sparrow, TRSP, n 13) and Fringilla montifringilla (Brambling, BRAM, n 8). All points represented = = individuals; polynomial curves are used to ft the trends of each species

migrants had high- efciency wings for long-journey Reduction in the fight speed resulted in decreased fight, and residents had high-maneuverability wings for parasite drag, which could prevent extra fight energy escaping, foraging, etc. (Minias et al. 2015; Grilli et al. consumption (Pennycuick 2008). Similarly, we found 2017). Lowered wingbeat frequency and wing stroke the BRAM exhibited reduced Vmr and Vmax, and their amplitude for BRAM relative to TRSP can be an adapta- corresponding parasite drag, Reynolds number, and tion for optimizing energy efciency since aerodynamic efciency of transport (mass-corrected power cost per power output (Ellington 1984; Pennycuick 2008) and 100 km) relative to the TRSP. Te BRAM had a higher metabolic rates (Bishop et al. 2015) are declining super- energy efciency of fight, especially at a low- and mid- linearly with the wingbeat frequency and stroke ampli- dle- speed range (Fig. 5), which may be an ecological tude. Lowered wing loading of BRAM would require a strategy for reducing extra energy cost during taking- reduced wingbeat frequency and stroke amplitude to stay of and escaping fight. By contrast, the TRSP with sig- airborne, which could be one of the reasons that BRAM nifcantly higher power may be essential to enhance the showed higher efciency of powered fight for long-dis- fight speed range (Askew and Ellerby 2007), since the tance migration. Our results provided evidence that the residents cannot mitigate the competition and preda- migratory passerines exhibit a higher fight energy ef- tion through seasonal migration. Terefore, migrant ciency, especially at a lower speed range, and this func- passerines enhanced fight energy efciency not only tional improvement is evolved through the combined through lowering fight speed but energy efciency adaptive features of wing morphology and kinematics. at a given speed, resulting from a suite of alternations in function-based morphology and kinematics Wang et al. Avian Res (2020) 11:25 Page 8 of 9

(mentioned above) relative to residents. Our results Ethics approval and consent to participate All protocols were approved by the Ethics and Animal Welfare Committee (no. further suggest that migrants would increase their 2013-6) and by the Institutional Animal Care and Use Committee (HEBTU2013- fight efciency without compromising fight maneu- 7) of Hebei Normal University, China, and were carried out under the auspices verability during takeof since the vertical speed and of scientifc collecting permits issued by the Department of Wildlife Conserva- tion (Forestry Bureau) of Hebei Province, China. power margin are comparable between migrants and residents. However, lower maximum speed for the Consent for publication migrants may also decrease the success rates of escape Not applicable. in extreme conditions compared with residents (Clem- Competing interests ente and Wilson 2016). The authors declare that they have no competing interests.

Conclusions Author details 1 Key Laboratory of Animal Physiology, Biochemistry and Molecular Biol- In summary, our results indicate that migrants exhibit ogy of Hebei Province, College of Life Sciences, Hebei Normal University, 2 the feature of reduced fight power with the lower Shijiazhuang 050024, China. Ocean College of Hebei Agricultural University, Qinhuangdao 066003, China. cost for fight energy and maneuverability. On the other hand, residents exhibit the opposite direction of Received: 29 February 2020 Accepted: 12 July 2020 increasing fight power that is critical for enhancing maximum fight speed and power to widen speed range for predator escaping and local competition. Our fnd- ings support the notion that migratory passerines have References Alerstam T. Optimal bird migration revisited. J Ornithol. 2011;152:5–23. acquired a better airborne energy efciency through a Alerstam T, Rosén M, Bäckman J, Ericson PG, Hellgren O. Flight speeds among series of adaptive changes on fight-related morphology bird species: allometric and phylogenetic efects. PLoS Biol. 2007;5:e197. and kinematics. However, these morphological and kin- Altshuler DL, Dudley R, McGuire JA. Resolution of a paradox: hummingbird fight at high elevation does not come without a cost. Proc Natl Acad ematic adaptations are still not enough to increase both Sci USA. 2004;101:17731–6. fight speed and efciency concurrently. Migrants are Altshuler D, Dudley R, Heredia S, McGuire J. Allometry of hummingbird lift- under the selection of balancing time and energy con- ing performance. J Exp Biol. 2010;213:725–34. Askew GN, Ellerby DJ. The mechanical power requirements of avian fight. sumption of the long-distance migration during their Biol Lett. 2007;3:445–8. long-distance migration (energy seems more vital for Bauchinger U, Both C, Piersma T. Are there specifc adaptations for long- BRAM). Further investigations are needed to include distance migration in birds? The search for adaptive syndromes—out- line of the European Science Foundation Workshop. Ann NY Acad Sci. multiple avian taxonomies for exploring potential phy- 2005;1046:214–5. logenetic efects and their metabolic and molecular Bauer S, Hoye BJ. Migratory animals couple biodiversity and ecosystem alternations to expand our understanding of evolution functioning worldwide. Science. 2014;344:1242552. Bishop CM, Spivey RJ, Hawkes LA, Batbayar N, Chua B, Frappell PB, et al. The in the efciency of airborne travel. roller coaster fight strategy of bar-headed geese conserves energy during Himalayan migrations. Science. 2015;347:250–4. Supplementary information Chernetsov N. Optimal migration theory. Berlin: Springer; 2012. p. 19–50. Supplementary information accompanies this paper at https://doi. Clemente CJ, Wilson RS. Speed and maneuverability jointly determine org/10.1186/s40657-020-00211-y. escape success: exploring the functional bases of escape performance using simulated games. Behav Ecol. 2016;27:45–54. Dudley R. Biomechanics of fight in neotropical butterfies: aerodynamics Additional fle 1: Movie S1. TRSP top view. and mechanical power requirements. J Experim Biol. 1991;159:335–57. Ellington C. The aerodynamics of hovering insect fight. III. Kinematics. Additional fle 2: Movie S2. TRSP side view. Philos T R Soc B. 1984;305:41–78. Fang KL, Li XD, Guo YM, Li F, Yu XD. Migration of brambling (Fringilla montifringilla) in Gaofeng forestry area of Nenjiang district. Chin J Wildlife. Acknowledgements 2008;29:121–3. We appreciate the help of Mr. Guanqun Kou for sample and video collection. Gavrilov VM. Energy expenditures for fight, aerodynamic quality, and coloniza- tion of forest habitats by birds. Biol Bull. 2011;38:779–88. Authors’ contributions Grilli MG, Lambertucci SA, Therrien JF, Bildstein KL. Wing size but not wing DL and YWu conceived the ideas and designed the study; YWang, YY, ZP, YS, shape is related to migratory behavior in a soaring bird. J Avian Biol. and JL conducted the experiment and collected the data; YWang carried out 2017;48:669–78. the statistical analyses with the help of CJ; DL, YWu, and GN wrote the manu- Hedenström A. Aerodynamics, evolution and ecology of avian fight. Trends script. All authors read and approved the fnal manuscript. Ecol Evol. 2002;7:415–22. Hedenström A. Adaptations to migration in birds: behavioural strategies, mor- Funding phology and scaling efects. Philos T R Soc A. 2008;363:287–99. This study was funded by the National Natural Science Foundation of China Horton KG, Van Doren BM, La Sorte FA, Fink D, Sheldon D, Farnsworth A, (NSFC, 31672292) to DL, NSFC (31770445) to Y. Wu, NSFC (31800338) and the et al. Navigating north: how body mass and winds shape avian fight Foundation of Hebei Normal University (L042017B03) to Y. Wang. behaviours across a North American migratory fyway. Ecol Lett. 2018;21:1055–64. Availability of data and materials Klein HM, Johansson LC, Hedenstrom A. Power of the wingbeat: modelling Our additional materials are available online. the efects of fapping wings in vertebrate fight. Proc R Soc Lond A. 2015;471:20140952. Wang et al. Avian Res (2020) 11:25 Page 9 of 9

Li M, Zhu W, Wang Y, Sun Y, Li J, Liu X, et al. Efects of capture and captivity on Sun Y, Ren Z, Wu Y, Lei F, Dudley R, Li D. Flying high: limits to fight performance plasma corticosterone and metabolite levels in breeding Eurasian Tree by sparrows on the Qinghai-Tibet Plateau. J Exp Biol. 2016;219:3642–8. Sparrows. Avian Res. 2019;10:16. Sun Y, Li M, Song G, Lei F, Li D, Wu Y. The role of climate factors in geographic Lockwood R. Avian wingtip shape reconsidered: wingtip shape indices and variation in body mass and wing length in a passerine bird. Avian Res. morphological adaptations to migration. J Avian Biol. 1998;29:273–92. 2017;8:1. Marden H. Maximum lift production during takeof in fying animals. J Exp Biol. Tobalske BW, Hedrick TL, Biewener AA. Wing kinematics of avian fight across 1987;130:235–58. speeds. J Avian Biol. 2003;34:177–84. Minias P, Meissner W, Wlodarczyk R, Ozarowska A, Piasecka A, Kaczmarek K, van Oorschot BK, Mistick EA, Tobalske BW. Aerodynamic consequences of et al. Wing shape and migration in shorebirds: a comparative study. Ibis. wing morphing during emulated takeof and gliding in birds. J Exp Biol. 2015;157:528–35. 2016;219:3146–54. Nilsson C, Klaassen RHG, Alerstam T. Diferences in speed and duration of bird Vincze O, Vagasi CI, Pap PL, Palmer C, Moller AP. Wing morphology, fight type migration between spring and autumn. Am Nat. 2013;181:837–45. and migration distance predict accumulated fuel load in birds. J Exp Biol. Pennycuick CJ. Modelling the fying bird. London: Academic Press; 2008. 2018;222:jeb183517. R Core Team. R: a language and environment for statistical computing. R Wang Y, Yin Y, Ge SY, Li M, Zhang Q, Li JY, et al. Limits to load-lifting perfor- foundation for statistical computing, Vienna; 2018. https://www.R-proje mance in a passerine bird: the efects of intraspecifc variation in mor- ct.org/. phological and kinematic parameters. PeerJ. 2019;7:e8048. Schmaljohann H. Proximate mechanisms afecting seasonal diferences in Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT. Links between worlds: migration speed of avian species. Sci Rep. 2018;8:4106. unraveling migratory connectivity. Trends Ecol Evol. 2002;17:76–83. Snow DW, Perrins CM. The birds of the Western Palearctic, volume 2: Passer- Zhao M, Christie M, Coleman J, Hassell C, Gosbell K, Lisovski S, et al. Time ines. Oxford: Oxford University Press; 1998. versus energy minimization migration strategy varies with body size and Summers-Smith D. Eurasian tree sparrow (Passer montanus). In: del Hoyo J, season in long-distance migratory shorebirds. Mov Ecol. 2017;5:23. Elliott A, Sargatal J, Christie DA, de Juana E, editors. Handbook of the birds of the World Alive. Barcelona: Lynx edicions; 2016.

Ready to submit your research ? Choose BMC and benefit from:

• fast, convenient online submission • thorough peer review by experienced researchers in your ﬁeld • rapid publication on acceptance • support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations • maximum visibility for your research: over 100M website views per year

At BMC, research is always in progress.

Learn more biomedcentral.com/submissions